scholarly journals Responses of thalamic neurons to itch- and pain-producing stimuli in rats

2018 ◽  
Vol 120 (3) ◽  
pp. 1119-1134 ◽  
Author(s):  
Brett Lipshetz ◽  
Sergey G. Khasabov ◽  
Hai Truong ◽  
Theoden I. Netoff ◽  
Donald A. Simone ◽  
...  

Understanding of processing and transmission of information related to itch and pain in the thalamus is incomplete. In fact, no single unit studies of pruriceptive transmission in the thalamus have yet appeared. In urethane-anesthetized rats, we examined responses of 66 thalamic neurons to itch- and pain- inducing stimuli including chloroquine, serotonin, β-alanine, histamine, and capsaicin. Eighty percent of all cells were activated by intradermal injections of one or more pruritogens. Forty percent of tested neurons responded to injection of three, four, or even five agents. Almost half of the examined neurons had mechanically defined receptive fields that extended onto distant areas of the body. Pruriceptive neurons were located within what appeared to be a continuous cell column extending from the posterior triangular nucleus (PoT) caudally to the ventral posterior medial nucleus (VPM) rostrally. All neurons tested within PoT were found to be pruriceptive. In addition, neurons in this nucleus responded at higher frequencies than did those in VPM, an indication that PoT might prove to be a particularly interesting region for additional studies of itch transmission. NEW & NOTEWORTHY Processing of information related to itch within in the thalamus is not well understood, We show in this, the first single-unit electrophysiological study of responses of thalamic neurons to pruritogens, that itch-responsive neurons are concentrated in two nuclei within the rat thalamus, the posterior triangular, and the ventral posterior medial nuclei.

1997 ◽  
Vol 78 (3) ◽  
pp. 1691-1706 ◽  
Author(s):  
Miguel A. L. Nicolelis ◽  
Rick C. S. Lin ◽  
John K. Chapin

Nicolelis, Miguel A. L., Rick C. S. Lin, and John K. Chapin. Neonatal whisker removal reduces the discrimination of tactile stimuli by thalamic ensembles in adult rats. J. Neurophysiol. 78: 1691–1706, 1997. Simultaneous recordings of up to 48 single neurons per animal were used to characterize the long-term functional effects of sensory plastic modifications in the ventral posterior medial nucleus (VPM) of the thalamus following unilateral removal of facial whiskers in newborn rats. One year after this neonatal whisker deprivation, neurons in the contralateral VPM responded to cutaneous stimulation of the face at much longer minimal latencies (15.2 ± 8.2 ms, mean ± SD) than did normal cells (8.8 ± 5.3 ms) in the same subregion of the VPM. In 69% of these neurons, the initial sensory responses to stimulus offset were followed for up to 700 ms by reverberant trains of bursting discharge, alternating in 100-ms cycles with inhibition. Receptive fields in the deafferented VPM were also atypical in that they extended over the entire face, shoulder, forepaw, hindpaw, and even ipsilateral whiskers. Discriminant analysis (DA) was then used to statistically evaluate how this abnormal receptive field organization might affect the ability of thalamocortical neuronal populations to “discriminate” somatosensory stimulus location. To standardize this analysis, three stimulus targets (“groups”) were chosen in all animals such that they triangulated the central region of the “receptive field” of the recorded multineuronal ensemble. In the normal animals these stimulus targets were whiskers or perioral hairs; in the deprived animals the targets typically included hairy skin of the body as well as face. The measured variables consisted of each neuron's spiking response to each stimulus differentiated into three poststimulus response epochs (0–15, 15–30, and 30–45 ms). DA quantified the statistical contribution of each of these variables to its overall discrimination between the three stimulus sites. In the normal animals, the stimulus locations were correctly classified in 88.2 ± 3.7% of trials on the basis of the spatiotemporal patterns of ensemble activity derived from up to 18 single neurons. In the deprived animals, the stimulus locations were much less consistently discriminated (reduced to 73.5 ± 12.6%; difference from controls significant at P < 0.01) despite the fact that much more widely spaced stimulus targets were used and even when up to 20 neurons were included in the ensemble. Overall, these results suggest that neonatal damage to peripheral sense organs may produce marked changes in the physiology of individual neurons in the somatosensory thalamus. Moreover, the present demonstration that these changes can profoundly alter sensory discrimination at the level of neural populations in the thalamus provides important evidence that the well-known perceptual effects of chronic peripheral deprivation may be partially attributable to plastic reorganization at subcortical levels.


2008 ◽  
Vol 100 (2) ◽  
pp. 681-689 ◽  
Author(s):  
Radi Masri ◽  
Tatiana Bezdudnaya ◽  
Jason C. Trageser ◽  
Asaf Keller

In all sensory systems, information is processed along several parallel streams. In the vibrissa-to-barrel cortex system, these include the lemniscal system and the lesser-known paralemniscal system. The posterior medial nucleus (POm) is the thalamic structure associated with the latter pathway. Previous studies suggested that POm response latencies are positively correlated with stimulation frequency and negatively correlated with response duration, providing a basis for a phase locked loop-temporal decoding of stimulus frequency. We tested this hypothesis by analyzing response latencies of POm neurons, in both awake and anesthetized rats, to vibrissae deflections at frequencies between 0.3 and 11 Hz. We found no significant, systematic correlation between stimulation frequency and the latency or duration of POm responses. We obtained similar findings from recording in awake rats, in rats under different anesthetics, and in anesthetized rats in which the reticular activating system was stimulated. These findings suggest that stimulus frequency is not reliably reflected in response latency of POm neurons. We also tested the hypothesis that POm neurons respond preferentially to sensor motion, that is, they respond to whisking in air, without contacts. We recorded from awake, head-restrained rats while monitoring vibrissae movements. All POm neurons responded to passive whisker deflections, but none responded to noncontact whisking. Thus like their counterparts in the trigeminal ganglion, POm neurons may not reliably encode whisking kinematics. These observations suggest that POm neurons might not faithfully encode vibrissae inputs to provide reliable information on vibrissae movements or contacts.


2021 ◽  
Vol 118 (30) ◽  
pp. e2104137118
Author(s):  
Vandana Sampathkumar ◽  
Andrew Miller-Hansen ◽  
S. Murray Sherman ◽  
Narayanan Kasthuri

Higher order thalamic neurons receive driving inputs from cortical layer 5 and project back to the cortex, reflecting a transthalamic route for corticocortical communication. To determine whether or not individual neurons integrate signals from different cortical populations, we combined electron microscopy “connectomics” in mice with genetic labeling to disambiguate layer 5 synapses from somatosensory and motor cortices to the higher order thalamic posterior medial nucleus. A significant convergence of these inputs was found on 19 of 33 reconstructed thalamic cells, and as a population, the layer 5 synapses were larger and located more proximally on dendrites than were unlabeled synapses. Thus, many or most of these thalamic neurons do not simply relay afferent information but instead integrate signals as disparate in this case as those emanating from sensory and motor cortices. These findings add further depth and complexity to the role of the higher order thalamus in overall cortical functioning.


1965 ◽  
Vol 209 (2) ◽  
pp. 307-311 ◽  
Author(s):  
S. T. Kitai ◽  
H. Ha ◽  
F. Morin

The lateral cervical nucleus (LCN) of the dog ( Canis familiaris) was investigated by histological and microelectrode technique. The LCN extends from the obex to the upper C3 and is located ventrolateral to the dorsal horn. Cell counts showed over 6,000 cells in the nuclei on both sides and the cell size varied from 20 to 45 µ. Single-unit analysis of the 220 neurons showed that the majority of cells responded to touch, some to pressure, some to pressure and touch, and an extremely limited number to joint movement. All responses were recorded from the ipsilateral half of the body. More than half of these neurons had small peripheral receptive fields located mostly in the distal parts of the limbs. The rest, with large receptive fields, were located mainly in the proximal parts of the limbs and the trunk. The peripheral receptive fields were almost equally distributed among the forelimb, trunk, and hindlimb for touch. The prominence of the hindlimb representation over the forelimb was found for pressure and for touch and pressure. The results indicate that the organization of the afferent input to the LCN has some similarity to that of the medial lemniscus system.


1993 ◽  
Vol 70 (2) ◽  
pp. 482-491 ◽  
Author(s):  
J. Bruggemann ◽  
C. Vahle-Hinz ◽  
K. D. Kniffki

1. In alpha-chloralose-anesthetized cats the region surrounding the ventral posterolateral nucleus (VPL) of the thalamus was investigated to locate foci with input from the urinary bladder stimulated by application of intravesical pressure. The locations of the recording sites were verified in Nissl-stained histological sections with reference to electrolytic lesions. 2. Of the 23 visceroceptive thalamic neurons identified, 4 (17%) were located in the periphery of the VPL (VPLp) and 19 (83%) in the lateral and dorsal aspects of the posterior complex (POl and POd, respectively) adjoining VPLp. 3. The neurons responded to noxious intensities of intravesical pressure in the range of 50-100 mmHg. Excitatory responses were elicited in 8 (35%) neurons, "inhibitory" responses in 13 (57%) neurons, and 2 (9%) neurons responded with an increase and a decrease of their discharge to subsequent stimuli. 4. Of the 22 visceroceptive thalamic neurons tested for this parameter, 73% had low-threshold cutaneous receptive fields (RFs). These were located in the region of the lower back, the hip, the thigh, and the proximal tail (12 PO neurons), or covered the entire postcranial contralateral part of the body (3 PO neurons). For only one of the VPLp neurons, a somatic RF was found and this was located on the distal tail. The neurons responded to tap stimuli applied at a low repetition rate. None of the 11 neurons tested with noxious pinching of the skin was activated by this kind of stimulus. 5. It is concluded that the cat's lateral thalamic region, around but not within VPL proper, contains neurons that play a role in the processing of information about noxious events in the urinary bladder. A comparison with results from experiments in the monkey indicates differences in the organization of the visceroceptive systems between both species, regarding the thalamic localization of visceroceptive neurons, the occurrence of convergent low-threshold somatic RFs, and the association of excitatory and inhibitory effects of urinary bladder stimulation with the location of somatic RFs.


1983 ◽  
Vol 50 (4) ◽  
pp. 910-925 ◽  
Author(s):  
H. R. Clemo ◽  
B. E. Stein

The organization of sensory representations in the cortex of the anterior ectosylvian sulcus (AES) of the cat was investigated using single-unit recording techniques. Somatic, auditory, and visual cells were found in the AES but were partially segregated. Somatic cells were concentrated in the rostral two-thirds of the sulcus, auditory cells were found in the caudal third, and visual cells were distributed along the fundus. A distinct, heretofore unknown, somatotopic representation of the body surface was observed in the AES and was designated SIV. The representation of the body in SIV extends along a rostrocaudal axis and the entire somatotopic map is inverted, with the head rostral and the hindquarters caudal. The representation of the paws extends over the lip of the sulcus to abut the paw representations in SII, and the SIV-SII boundary is marked by a reversal in the sequence of receptive fields along the AEG-AES. The SIV representation (SII) on the crown of the anterior ectosylvian gyrus (AEG). The somatotopic map in SII was found to extend further lateral on the AEG than shown by some investigations and it contains a double representation of the limbs: a large representation with the limbs having the opposite orientation to and abutting the SIV map and a smaller representation located more medial on the AEG and extending into the suprasylvian sulcus. The presence of this double representation may help to explain previous discrepancies regarding the overall orientation of the body in SII.


1996 ◽  
Vol 76 (1) ◽  
pp. 130-140 ◽  
Author(s):  
J. C. Brumberg ◽  
D. J. Pinto ◽  
D. J. Simons

1. Extracellular single-unit recordings and controlled whisker stimuli were used to compare response properties of cells in the barreloids of the ventral posterior medial nucleus of the thalamus and the barrels in the rat primary somatosensory cortex. Whiskers were deflected alone or in combinations involving up to four immediately adjacent whiskers to assess their relative inhibitory and excitatory contributions to individual receptive fields. Quantitative data were obtained from 51 thalamocortical units (TCUs), 79 "regular-spiking" barrel neurons (RSUs), and 5 "fast-spiking" barrel neurons (FSUs) in 28 normal female adult rats. 2. A random-noise generator was used to produce small, continuously varying whisker movements that were applied to one to four adjacent whiskers while the principal (columnar) whisker was displaced with the use of a ramp-and-hold deflection. RSUs displayed adjacent whisker-evoked inhibition that increased as the number of adjacent whiskers stimulated was incremented. Asymptotic levels of inhibition were reached with the application of the noise stimulus to two or three adjacent whiskers depending on which particular combinations were deflected. By contrast, TCUs and FSUs showed weak, or no, surround inhibition. 3. As the number of adjacent whiskers stimulated increased, the background (prestimulus) activity in TCUs and FSUs increased, whereas displayed background activity in RSUs was relatively unaffected. The increase in background activity observed in the FSUs is hypothesized to mediate adjacent whisker-evoked inhibition in the RSUs. 4. A spatial gradient of adjacent whisker inhibition was observed in RSUs. The caudally adjacent whisker evoked more inhibition than the rostrally adjacent whisker, and the ventral more than the dorsal. A cortical origin for the gradient is suggested by the finding that TCUs did not show a spatial inhibitory gradient. 5. As the noise stimulus was applied to an increasing number of adjacent whiskers, RSUs became more sharply tuned for deflection angles. Neither TCUs nor FSUs showed increases in angular tuning. 6. Inhibition worked disproportionately in RSUs to inhibit those responses that were initially the least robust. For example, inhibition was most effective at reducing responses to nonpreferred versus preferred whisker deflection angles. 7. To assess the principal whisker's effect on adjacent whisker excitatory responses, the noise stimulus was applied to the principal whisker. In RSUs, principal whisker-evoked inhibition was more potent than adjacent whisker-evoked inhibition. FSUs were excited to a greater extent by the application of the noise stimulus to the principal whisker than to adjacent whiskers. TCUs did not display principal whisker-evoked inhibition. 8. Inhibition within the barrel serves as a contrast enhancement mechanism to differentiate small versus large magnitude responses. Less vigorous responses, such as those associated with perturbations of noncolumnar whiskers and inputs from nonoptimal deflection angles, are more strongly suppressed. During active touch, when many whiskers simultaneously palpate an object, these inhibitory interactions could effectively increase the "principal whiskerness" of the cortical column.


2016 ◽  
Vol 116 (3) ◽  
pp. 1261-1274 ◽  
Author(s):  
Amanda K. Kinnischtzke ◽  
Erika E. Fanselow ◽  
Daniel J. Simons

The functional role of input from the primary motor cortex (M1) to primary somatosensory cortex (S1) is unclear; one key to understanding this pathway may lie in elucidating the cell-type specific microcircuits that connect S1 and M1. Recently, we discovered that a subset of pyramidal neurons in the infragranular layers of S1 receive especially strong input from M1 (Kinnischtzke AK, Simons DJ, Fanselow EE. Cereb Cortex 24: 2237–2248, 2014), suggesting that M1 may affect specific classes of pyramidal neurons differently. Here, using combined optogenetic and retrograde labeling approaches in the mouse, we examined the strengths of M1 inputs to five classes of infragranular S1 neurons categorized by their projections to particular cortical and subcortical targets. We found that the magnitude of M1 synaptic input to S1 pyramidal neurons varies greatly depending on the projection target of the postsynaptic neuron. Of the populations examined, M1-projecting corticocortical neurons in L6 received the strongest M1 inputs, whereas ventral posterior medial nucleus-projecting corticothalamic neurons, also located in L6, received the weakest. Each population also possessed distinct intrinsic properties. The results suggest that M1 differentially engages specific classes of S1 projection neurons, thereby regulating the motor-related influence S1 exerts over subcortical structures.


1969 ◽  
Vol 50 (1) ◽  
pp. 129-140 ◽  
Author(s):  
M. S. LAVERACK

1. Mechanoreceptors in the body wall of the leech Hirudo are stimulated by deformation of the animal's surface. They respond at all frequencies of stimulation up to about 50-60 Hz. 2. Light flashes, from a microscope lamp or an electronic flash source, are also a potent means of peripheral stimulation. 3. After peripheral stimulation impulses can be recorded in a fast central pathway. This pathway conducts equally well in the posterior to anterior and in the opposite directions. 4. Interference with either the right or left connective linking any two segmental ganglia does not interrupt the rapid conduction of these impulses. 5. Severance of the median connective or Faivre's nerve interrupts conduction. This seems to implicate at least one, and possibly more, of the nerve fibres of this median connective in the rapid transmission of information from the extremities of the body. 6. A slower conducting pathway also exists in the nerve cord.


2008 ◽  
Vol 99 (1) ◽  
pp. 356-366 ◽  
Author(s):  
Michael Shoykhet ◽  
Daniel J. Simons

Extracellular single-unit recordings were used to characterize responses of thalamic barreloid and cortical barrel neurons to controlled whisker deflections in 2, 3-, and 4-wk-old and adult rats in vivo under fentanyl analgesia. Results indicate that response properties of thalamic and cortical neurons diverge during development. Responses to deflection onsets and offsets among thalamic neurons mature in parallel, whereas among cortical neurons responses to deflection offsets become disproportionately smaller with age. Thalamic neuron receptive fields become more multiwhisker, whereas those of cortical neurons become more single-whisker. Thalamic neurons develop a higher degree of angular selectivity, whereas that of cortical neurons remains constant. In the temporal domain, response latencies decrease both in thalamic and cortical neurons, but the maturation time-course differs between the two populations. Response latencies of thalamic cells decrease primarily between 2 and 3 wk of life, whereas response latencies of cortical neurons decrease in two distinct steps—the first between 2 and 3 wk of life and the second between the fourth postnatal week and adulthood. Although the first step likely reflects similar subcortical changes, the second phase likely corresponds to developmental myelination of thalamocortical fibers. Divergent development of thalamic and cortical response properties indicates that thalamocortical circuits in the whisker-to-barrel pathway undergo protracted maturation after 2 wk of life and provides a potential substrate for experience-dependent plasticity during this time.


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